IL-10 indirectly modulates functional activity of CD4+CD28null T-lymphocytes through LFA-3 and HLA class II inhibition

Immunology. 2024 Oct;173(2):296-309. doi: 10.1111/imm.13824. Epub 2024 Jun 23.

Abstract

Expansion of CD4+CD28null T-lymphocytes is common in chronic heart failure (CHF) patients. Its ability to produce high levels of proinflammatory cytokines is probably the key role of these cells in CHF. IL-10 is a candidate for limiting CD4+CD28null T-lymphocyte responses, whereas tumour necrosis factor (TNF) is the cytokine most closely involved in the loss of CD28 expression. Serum levels of TNF and IL-10 were measured in 65 CHF patients (mean age, 65.2 ± 13.84 years). Patients with an IL-10/TNF ratio ≥1 had significantly lower levels of CD4+CD28null T-lymphocytes than those with a ratio <1. In vitro, IL-10 reduced the frequency of proliferative CD4+CD28null T-lymphocytes stimulated with anti-CD3. Pre-treatment with IL-10 before anti-CD3 stimulation was required for the cytokine to inhibit TNF production by CD4+CD28null T-lymphocytes. In addition to the previously described effect of IL-10 on HLA-DR and ICAM-1 expression, LFA-3 protein and mRNA levels were reduced in the presence of the cytokine in monocytes. IL-10 inhibition on CD4+CD28null T-lymphocytes may be mediated by a reduction in HLA class II and LFA-3 expression because blocking interactions with these costimulators has similar effects to those of IL-10 treatment. Moreover, costimulation through CD2/LFA-3 interaction is enough to induce proliferation and cytokine production in CD4+CD28null T-lymphocytes.

Keywords: T‐lymphocyte differentiation; chronic heart failure; immunosenescence.

MeSH terms

  • Aged
  • CD28 Antigens* / immunology
  • CD28 Antigens* / metabolism
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Cell Proliferation
  • Cells, Cultured
  • Female
  • HLA-DR Antigens / metabolism
  • Heart Failure / immunology
  • Heart Failure / metabolism
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • Interleukin-10* / metabolism
  • Lymphocyte Activation
  • Lymphocyte Activation Gene 3 Protein
  • Male
  • Middle Aged
  • Monocytes / immunology
  • Monocytes / metabolism
  • Tumor Necrosis Factor-alpha* / metabolism

Substances

  • Interleukin-10
  • CD28 Antigens
  • Tumor Necrosis Factor-alpha
  • Histocompatibility Antigens Class II
  • Lymphocyte Activation Gene 3 Protein
  • IL10 protein, human
  • Intercellular Adhesion Molecule-1
  • HLA-DR Antigens